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Susan Knowles

Publications and source records attributed to Susan Knowles.

At least 37 records · Page 2Linked to original sources

Mussel mass mortality and the microbiome: Evidence for shifts in the bacterial microbiome of a declining freshwater bivalve

Freshwater mussels (Unionida) are suffering mass mortality events worldwide, but the causes remain enigmatic. Here, we describe an analysis of bacterial loads, community structure, and inferred metabolic pathways in the hemolymph of pheasantshells ( Actinonaias pectorosa ) from the Clinch River, USA, during a multi-year mass mortality event. Bacterial loads were approximately 2 logs higher in moribund mussels (cases) than in apparently healthy mussels (controls). Bacterial communities also differed between cases and controls, with fewer sequence variants (SVs) and higher relative abundances of the proteobacteria Yokenella regensburgei and Aeromonas salmonicida in cases than in controls. Inferred bacterial metabolic pathways demonstrated a predominance of degradation, utilization, and assimilation pathways in cases and a predominance of biosynthesis pathways in controls. Only two SVs correlated with Clinch densovirus 1, a virus previously shown to be strongly associated with mortality in this system: Deinococcota and Actinobacteriota, which were associated with densovirus-positive and densovirus-negative mussels, respectively. Overall, our results suggest that bacterial invasion and shifts in the bacterial microbiome during unionid mass mortality events may result from primary insults such as viral infection or environmental stressors. If so, bacterial communities in mussel hemolymph may be sensitive, if generalized, indicators of declining mussel health.

Tennessee, Virginia

Experimental challenge of a North American bat species, big brown bat (Eptesicus fuscus), with SARS-CoV-2

The recently emerged novel coronavirus, SARS‐CoV‐2, is phylogenetically related to bat coronaviruses (CoVs), specifically SARS‐related CoVs from the Eurasian bat family Rhinolophidae. As this human pandemic virus has spread across the world, the potential impacts of SARS‐CoV‐2 on native North American bat populations are unknown, as is the ability of North American bats to serve as reservoirs or intermediate hosts able to transmit the virus to humans or to other animal species. To help determine the impacts of the pandemic virus on North American bat populations, we experimentally challenged big brown bats ( Eptesicus fuscus ) with SARS‐CoV‐2 under BSL‐3 conditions. We inoculated the bats both oropharyngeally and nasally, and over the ensuing three weeks, we measured infectivity, pathology, virus concentrations in tissues, oral and rectal virus excretion, virus transmission, and clinical signs of disease. We found no evidence of SARS‐CoV‐2 infection in any examined bat, including no viral excretion, no transmission, no detectable virus in tissues, and no signs of disease or pathology. Based on our findings, it appears that big brown bats are resistant to infection with the SARS‐CoV‐2. The potential susceptibility of other North American bat species to SARS‐CoV‐2 remains to be investigated.

Transboundary and Emerging Diseases

Domoic acid and saxitoxin in seabirds in the United States between 2007 and 2018

As harmful algal blooms (HABs) increase in magnitude and duration worldwide, they are becoming an expanding threat to marine wildlife. Over the past decade, blooms of algae that produce the neurotoxins domoic acid (DA) and saxitoxin (STX) and documented concurrent seabird mortality events have increased bicoastally in the United States. We conducted a retrospective analysis of HAB related mortality events in California, Washington, and Rhode Island between 2007 and 2018 involving 12 species of seabirds, to document the levels, ranges, and patterns of DA and STX in eight sample types (kidney, liver, stomach, intestinal, cloacal, cecal contents, bile, blood) collected from birds during these events. Samples ( n = 182 ) from 83 birds were examined for DA ( n = 135) or STX ( n = 17) or both toxins simultaneously ( n = 30), using ELISA or LCMS at the National Oceanographic and Atmospheric Administration, National Marine Fisheries Service (NOAA-NMFS) Wildlife Algal-toxin Research and Response Network (WARRN-West) or the University of California, Santa Cruz (UCSC). DA or STX was detected in seven of the sample types with STX below the minimum detection limit in blood for the three samples tested. DA was found in 70% and STX was found in 23% of all tested samples. The ranges of detectable levels of DA and STX in all samples were 0.65–681,190.00 ng g −1 and 2.00–20.95 ng g −1 , respectively. Cloacal contents from a Pacific loon ( Gavia pacifica ) collected in 2017 from Ventura County, California, had the highest maximum level of DA for all samples and species tested in this study. The highest level of STX for all samples and species was detected in the bile of a northern fulmar ( Fulmarus glacialis ) collected in 2018 from San Luis Obispo County, California. DA detections were consistently found in gastrointestinal samples, liver, bile, and kidney, whereas STX detections were most frequently seen in liver and bile samples. Co-occurring HAB toxins (DA and STX) were detected in white-winged scoters ( Melanitta deglandi ) in 2009, a Brandt's cormorant ( Phalacrocorax penicillatus ) in 2015, and a northern fulmar and common murre ( Uria aalge ) in 2018. This article provides DA and STX tissue concentrations and patterns in avian samples and shows the utility of various sample types for the detection of HAB toxins. Future research to understand the pharmacodynamics of these toxins in avian species and to establish lethal doses in various bird species would be beneficial.

Harmful Algae

Investigation of algal toxins in a multispecies seabird die-off in the Bering and Chukchi seas

Between 2014 and 2017, widespread seabird mortality events were documented annually in the Bering and Chukchi seas, concurrent with dramatic reductions of sea ice, warmer than average ocean temperatures, and rapid shifts in marine ecosystems. Among other changes in the marine environment, harmful algal blooms (HABs) that produce the neurotoxins saxitoxin (STX) and domoic acid (DA) have been identified as a growing concern in this region. Although STX and DA have been documented in Alaska (US) for decades, current projections suggest that the incidence of HABs is likely to increase with climate warming and may pose a threat to marine birds and other wildlife. In 2017, a multispecies die-off consisting of primarily Northern Fulmars ( Fulmarus glacialis ) and Short-tailed Shearwaters ( Ardenna tenuirostris ) occurred in the Bering and Chukchi seas. To evaluate whether algal toxins may have contributed to bird mortality, we tested carcasses collected from multiple locations in western and northern Alaska for STX and DA. We did not detect DA in any samples, but STX was present in 60% of all individuals tested and in 88% of Northern Fulmars. Toxin concentrations in Northern Fulmars were within the range of those reported from other STX-induced bird die-offs, suggesting that STX may have contributed to mortalities. However, direct neurotoxic action by STX could not be confirmed and starvation appeared to be the proximate cause of death among birds examined in this study.

Journal of Wildlife Diseases

Pathology of Lagovirus europaeus GI.2/RHDV2/b (rabbit hemorrhagic disease virus 2) in native North American lagomorphs

Rabbit hemorrhagic disease, a notifiable foreign animal disease in the US, was reported for the first time in wild native North American lagomorphs in April 2020 in the southwestern US. Affected species included the desert cottontail ( Sylvilagus audubonii ), mountain cottontail ( Sylvilagus nuttallii ), black-tailed jackrabbit ( Lepus californicus ), and antelope jackrabbit ( Lepus alleni ). Desert cottontails ( n =7) and black-tailed jackrabbits ( n =7) collected in April and May 2020 were necropsied at the US Geological Survey National Wildlife Health Center and tested positive for Lagovirus europaeus GI.2, also known as rabbit hemorrhagic disease virus 2 (GI.2/RHDV2/b), by real-time PCR at the US Department of Agriculture's Foreign Animal Disease Diagnostic Laboratory. Gross and microscopic lesions were similar to those reported in European rabbits ( Oryctolagus cuniculus ) and other hare ( Lepus ) species with GI.2/RHDV2/b infection; they included epistaxis (12/13; 92%); massive hepatocellular dissociation (14/14; 100%) and necrosis or apoptosis (11/11; 100%); pulmonary congestion (12/12; 100%), edema (12/13; 92%), and hemorrhage (11/12; 92%); and acute renal tubular injury (3/8; 38%). As in previous reports, massive hepatocellular dissociation and necrosis or apoptosis were the most diagnostically distinct finding. As North American Sylvilagus and Lepus species appear to be susceptible to fatal GI.2/RHDV2/b infection, additional work is needed to understand the host range, pathogenicity, and potential population effects of GI.2/RHDV2/b in North America.

Arizona, New Mexico, Texas

Mass mortality in freshwater mussels (Actinonaias pectorosa) in the Clinch River, USA, linked to a novel densovirus

Freshwater mussels (order Unionida) are among the world’s most biodiverse but imperiled taxa. Recent unionid mass mortality events around the world threaten ecosystem services such as water filtration, nutrient cycling, habitat stabilization, and food web enhancement, but causes have remained elusive. To examine potential infectious causes of these declines, we studied mussels in Clinch River, Virginia and Tennessee, USA, where the endemic and once-predominant pheasantshell ( Actinonaias pectorosa ) has suffered precipitous declines since approximately 2016. Using metagenomics, we identified 17 novel viruses in Clinch River pheasantshells. However, only one virus, a novel densovirus ( Parvoviridae ; Densovirinae ), was epidemiologically linked to morbidity. Clinch densovirus 1 was 11.2 times more likely to be found in cases (moribund mussels) than controls (apparently healthy mussels from the same or matched sites), and cases had 2.7 (log 10 ) times higher viral loads than controls. Densoviruses cause lethal epidemic disease in invertebrates, including shrimp, cockroaches, crickets, moths, crayfish, and sea stars. Viral infection warrants consideration as a factor in unionid mass mortality events either as a direct cause, an indirect consequence of physiological compromise, or a factor interacting with other biological and ecological stressors to precipitate mortality.

Virginia, Tennessee

Canine distemper virus in the sea otter population (Enhydra lutris) in Washington State, USA

Before 2001, all serosurveys for morbilliviruses in sea otters ( Enhydra lutris ) in California, Washington, and Alaska, USA, documented a 0% seroprevalence. The first published serologic detections of morbillivirus in sea otters occurred in 2001–02 in live-captured Washington sea otters, with a documented 80% seroprevalence. We conducted a retrospective study of sea otter cases from 1989 to 2010 compiled at the US Geological Survey, National Wildlife Health Center to identify cases of morbilliviral disease in Washington sea otters and to characterize the disease using immunohistochemistry, reverse transcription (RT)-PCR, genetic sequencing, virus isolation, and serology. We identified six cases of morbilliviral disease and 12 cases of morbilliviral infection in this population of sea otters during 2000–10. Significant histologic findings included inflammation in the white and gray matter of the brain characterized by lymphoplasmacytic perivascular cuffing, neuronal necrosis, and satellitosis in gray matter and by spongiosis, myelin degeneration, spheroids, and gemistocytes in white matter. Intranuclear and intracytoplasmic viral inclusion bodies were found in neurons, Purkinje cells, and glia. Immunohistochemistry for canine distemper virus (CDV) showed positive staining in neurons, glial cells, and cell processes. A pan-morbillivirus RT-PCR with subsequent restriction endonuclease digestion or sequencing identified CDV. Virus isolation was not successful. Two sea otters with morbilliviral encephalitis showed greater antibody titers to CDV than phocine distemper virus. Histologic changes were confined to the central nervous system and resembled neurologic canine distemper in domestic dogs. Cases of sea otters with morbilliviral infection without histologic changes could represent early infections or incompletely cleared sublethal infections. We found that morbillivirus was present in the Washington sea otter population as early as 2000, and we provide a description of the pathology of canine distemper in sea otters.

Washington

Environmental contamination and unusual snake mortality in an urban national wildlife refuge

The National Wildlife Refuge (NWR) System protects ~150 million acres of land and water in the United States and provides habitat for >2,000 native vertebrates species. Although legally protected, wildlife populations within these refuges can be threatened by anthropogenic activities. The lack of knowledge about such threats has the potential to undermine biodiversity conservation. We investigated patterns of wildlife mortality among three NWRs in the northern U.S. Gulf Coast. Visual surveys (958 total search-hours) were conducted for live or dead amphibians and reptiles at Big Branch, Bogue Chitto, and Bayou Sauvage NWRs. An exceptionally high incidence of snake mortality (>800% above background, P < 0.001) was observed at one site (Haul Road, Bayou Sauvage NWR). Mortality affected seven species and recurred for 29 months. Intact carcasses were subject to histopathological examination and diagnostic testing. Cause of death was undetermined (n = 9) or attributed to various pathogens (n = 5). To investigate possible underlying causes of this unusual mortality, water exposure challenges and soil toxicological analyses (n = 6 and 11 sites, respectively) were conducted on samples from Bayou Sauvage NWR, given the known potential for anthropogenic contamination in the refuge. In a controlled experiment, survival of Anaxyrus fowlerii embryos exposed to water from Recovery Road (i.e., 250m from a landfill) and Haul Road was reduced 92% and 48%, respectively, compared to four reference sites in the refuge. Sediment analyses suggested at least seven distinct sources of contaminants in Bayou Sauvage NWR. Potential sources included a landfill, illegal dumping, vehicle emissions, pesticide migration, and an active hydrocarbon pipeline leak discovered 600 m from Haul Road. Synthesis and applications: Although further research is needed to determine whether the observed mortality and contamination are related, these collective findings suggest that anthropogenic factors may threaten the ecological integrity of one of the United States largest urban wildlife refuges. More broadly, our study highlights the critical need for species inventories, baseline data, and systematic monitoring in NWRs. Such information is essential to detecting and mitigating anthropogenic threats to biodiversity conservation in protected areas.

Louisiana

Mortality of Tufted puffins (Fratercula cirrhata) and other alcids during an unusual mortality event in the eastern Bering Sea

Mass mortality events are increasing in frequency and magnitude, potentially linked with ongoing climate change. In October 2016 through January 2017, St. Paul Island situated at the shelf-edge of the Bering Sea, Alaska, experienced a mortality event of alcids (family: Alcidae), with over 350 carcasses recovered. Almost three-quarters of the carcasses were unscavenged, a rate much higher than in baseline surveys (17%), suggesting that a sudden, large deposition event overwhelmed local scavenger populations. Based on the observation that carcasses were not observed on the neighboring island of St. George, we bounded the at-sea distribution of moribund birds, and estimated all species mortality at 8,000 to 22,000 birds. The event was particularly anomalous given the late fall/winter timing of the event when low numbers of beached birds are typical; and the predominance of Tufted puffins (Fratercula cirrhata, 79% of carcass finds) and Crested auklets (Aethia cristatella, 11% of carcass finds), species that were nearly absent from long-term baseline surveys. Collected specimens were disease-free and severely emaciated, suggesting starvation as the ultimate cause of mortality. The majority (95%, N = 245) of Tufted puffins were regrowing flight feathers, indicating a potential contribution of molt stress. Immediately prior to this event, shifts in zooplankton community composition and forage fish distribution and energy density were documented in the eastern Bering Sea following a period of elevated sea surface temperatures, evidence cumulatively suggestive of a bottom-up shift in seabird prey availability. We posit that shifts in prey composition and distribution pushing birds outside of their normal fall migration pattern, combined with the onset of molt, resulted in this mortality event

Alaska

Lethal infection of wild raptors with highly pathogenic avian influenza H5N8 and H5N2 viruses in the USA, 2014–15

An outbreak of highly pathogenic avian influenza (HPAI) led to heavy losses of poultry in commercial farms in North America in 2014–15. Enhanced surveillance by virologists and pathologists at the US Geological Survey National Wildlife Health Center and its partners resulted in the identification of lethal infections with clade 2.3.4.4 subgroup icA2 H5N8 and novel reassortant H5N2 viruses in diverse wild raptor species that died concomitant with the poultry epizootic in the US. A range of pathologic abnormalities were present in dead raptors, including necrotizing encephalitis and myocarditis, pancreatic necrosis, and pulmonary congestion and edema. Raptors are highly susceptible to disease caused by infection with HPAI clade 2.3.4.4 viruses.

Journal of Wildlife Diseases

Leptospirosis in Northern Sea Otters (Enhydra lutris kenyoni) from Washington

We diagnosed leptospirosis in six northern sea otters ( Enhydra lutris kenyoni ) that stranded on beaches in Washington, US in 2002. Significant gross findings included cyanotic oral mucous membranes, renal swelling, congestion or pale streaks on the cut surface of the lobules, hematuria, dehydration, lymphadenopathy, pulmonary congestion and rarely adrenal hemorrhage and congestion. Histopathology showed lymphoplasmacytic tubulointerstitial nephritis with intraluminal spirochetes and immunoreactivity to leptospiral antigens in the renal tubules and interstitium. qPCR using kidney or urine for the leptospiral lipL32 gene was positive with cycle threshold values indicative of abundant or moderate amounts of nucleic acid. A microscopic agglutination test showed the highest serum antibody titer to serovar Pomona and titers to serovars Autumnalis, Bratislava, Hebdomadis, Grippo, Ictero, Pyrogenes, Ballum, Canicola, and Hardjo. While antibodies to Leptospira interrogans have been previously detected in sea otters, there are no reports of disease or descriptions of pathology.

Washington

An update on Toxoplasma gondii infections in northern sea otters (Enhydra lutris kenyoni) from Washington State, USA

Toxoplasmosis in marine mammals is epidemiologically and clinically important. Toxoplasma gondii antibodies (by modified agglutination test, cut-off ≥1:25) were detected in serum of 65 of 70 (92.9%) northern sea otters ( Enhydra lutris kenyoni ) from Washington State, USA. Brains and/or muscles of 44 sea otters were bioassayed in mice (INF-γ knock-out [KO], Swiss Webster outbred [SW]) and viable T. gondii was isolated from 22 of 44 (50%); T. gondii strains were lethal to KO mice but not SW mice. These T. gondii isolates were further propagated in cell culture. Multi-locus PCR-RFLP genotyping of cell culture-derived tachyzoites revealed four different genotypes among 22 isolates including ToxoDB PCR-RFLP genotype #5 (14 isolates), #1 (three isolates), #3 (four isolates), and #167 (one isolate). PCR-DNA sequencing based genotyping using polymorphic gene GRA6 revealed one of four different alleles. Among the 14 RFLP genotype #5 strains, 10 have GRA6 sequences that match with the Type A, one match with the Type X, two strains did not generate sequence data, and one strain had double peaks at known polymorphic sites indicating a mixed infection. The seven strains belong to genotypes #1 and #3, all have identical sequences to T. gondii Type II reference isolate ME49. Genotype #167 strain has identical sequence to Type I reference strain. In summary, we observed high seroprevalence, and high rate of isolation of T. gondii from northern sea otters and predominant genotype #5 that has been previously reported a dominant and widespread strain among terrestrial wildlife in North America. GRA6 sequence analysis of the genotype #5 isolates indicated the dominance of Type A lineage in sea otters in Washington State.

Washington

Mortality trends in northern sea otters (Enhydra lutris kenyoni) collected from the coasts of Washington and Oregon (2002–15)

During 2002−15 we examined the causes of mortality in a population of northern sea otters ( Enhydra lutris kenyoni ). Beachcast sea otters were collected primarily from the coast of Washington. Although there are no permanent sea otter residents in Oregon, several beachcast otters were collected from the Oregon coast. Infectious diseases were the primary cause of death (56%) for otters we examined. Sarcocystosis was the leading infectious cause of death (54%) and was observed throughout the study period. Some infectious diseases, such as morbilliviral encephalitis and leptospirosis, were documented for a limited number of years and then not detected again despite continued testing for these pathogens in necropsied animals. Trauma was the second most common cause of death (14%) during the study period. The continued stable growth of the Washington population of otters suggests they are able to tolerate current mortality rates.

Oregon, Washington

Chlamydia psittaci in feral Rosy-faced Lovebirds (Agapornis roseicollis) and other backyard birds in Maricopa County, Arizona

In 2013, a mortality event of nonnative, feral Rosy-faced Lovebirds ( Agapornis roseicollis ) in residential backyards in Maricopa County, Arizona, US was attributed to infection with Chlamydia psittaci . In June 2014, additional mortality occurred in the same region. Accordingly, in August 2014 we sampled live lovebirds and sympatric bird species visiting backyard bird feeders to determine the prevalence of DNA and the seroprevalence of antibodies to C. psittaci using real-time PCR-based testing and elementary body agglutination, respectively. Chlamydia psittaci DNA was present in conjunctival-choanal or cloacal swabs in 93% (43/46) of lovebirds and 10% (14/142) of sympatric birds. Antibodies to C. psittaci were detected in 76% (31/41) of lovebirds and 7% (7/102) of sympatric birds. Among the sympatric birds, Rock Doves ( Columba livia ) had the highest prevalence of C. psittaci DNA (75%; 6/8) and seroprevalence (25%; 2/8). Psittacine circovirus 1 DNA was also identified, using real-time PCR-based testing, from the same swab samples in 69% (11/16) of species sampled, with a prevalence of 80% (37/46) in lovebirds and 27% (38/142) in sympatric species. The presence of either Rosy-faced Lovebirds or Rock Doves at residential bird feeders may be cause for concern for epizootic and zoonotic transmission of C. psittaci in this region.

Arizona

Infectious canine hepatitis in a brown bear (Ursus arctos horribilis) from Alaska.

We diagnosed infectious canine hepatitis in a free-ranging brown bear ( Ursus arctos horribilis ) cub from Alaska, US, found dead in October 2015. Intranuclear inclusion bodies were present in hepatocytes, and immunohistochemistry showed reactivity to adenoviral antigens. Sequencing of the hexon protein of adenovirus showed 100% identity to canine adenovirus 1.

Journal of Wildlife Diseases

Building a response network to investigate potential pathogens associated with unionid mortality events

Unexplained mortality events have confounded the mussel conservation community for over 30 years. While the effects of chemical pollutants and environmental factors have been examined, few investigations have focused on the identification of potential mussel pathogens. Consequently, very little is known regarding the impact that pathogens have on freshwater mussel health, especially as they pertain to propagation efforts. There are several barriers that have hindered progress in the study of freshwater mussel disease, one of which is lack of appropriate diagnostic tools, and another is lack of guidance for field personnel regarding sampling procedures and laboratory contacts.

Ellipsaria